Antibiosis and Non-preference of Sitobion avenae (F.) (Hemiptera: Aphididae) on Leaves and Ears of Commercial Cultivars of Wheat (Triticum aestivum)

Little is known on the resistance of wheat cultivars to Sitobion avenae (F.) in Brazil. The goal of this work was to assess the behavior and biology of S. avenae on four commercial wheat cultivars to verify the existence of resistance by antibiosis in leaves and ears and non-preference in the ears. The smallest net fecundity rates of S. avenae in wheat leaves have been found in the cultivars Embrapa 22 and BRS264, which did not differ between themselves. The intrinsic rate of increase of S. avenae was smaller in leaves of Embrapa 22 than in cultivars BRS254 and BRS Timbaúva. The smallest net fecundity rates of S. avenae in wheat ears were observed in the cultivars BRS254 and Embrapa 22. The intrinsic rate of increase of the aphid in the ear of cultivar Embrapa 22 was smaller than in BRS Timbaúva and BRS264, but did not differ from BRS254. The organ of the wheat plant in which the aphid was reared influences antibiosis resistance, but the cultivar BRS Timbaúva was considered susceptible and Embrapa 22 resistant to S. avenae in both plant organs tested. Ears of wheat cultivars tested did not show differences in the mechanism of resistance by non-preference to S. avenae.     

Assessment of Sublethal and Transgenerational Effects of Pirimicarb on the Wheat Aphids Rhopalosiphum padi and Sitobion avenae

The wheat aphids, Rhopalosiphum padi (Linnaeus) and Sitobion avenae (Fabricius), are key pests on wheat crops worldwide. Management practices rely primarily on insecticides. The pirimicarb (carbamate) is used extensively as an effective insecticide to control these two aphids. In addition to the mortality caused by pirimicarb, various sublethal effects may occur in aphids when exposed to low lethal or sublethal doses. Understanding the general effect of pirimicarb on aphids could help increasing rational use of this insecticide. Under laboratory conditions, we assessed the sublethal effects of a low lethal concentration of pirimicarb (LC₂₅) on biological traits and acetylcholinesterase (AChE) activity of R. padi and S. avenae. Both direct and transgenerational effects, i.e. on parent and the F1 generations were assessed, respectively. We found that R. padi and S. avenae responded differentially to the LC₂₅ of pirimicarb. The parent generation of R. padi showed a 39% decrease in fecundity and multiple transgenerational effects were observed in the F1 generation; overall juvenile development, reproductive period, adult longevity and lifespan were longer than those of the control group. By contrast, LC₂₅ of pirimicarb showed almost no effects on S. avenae biological traits in both the parent and F1 generations; only the pre-reproductive duration was reduced in F1 generations. Demographic parameter estimates (e.g. r_m) showed similar trend, i.e. significant negative effect on R. padi population growth and no effect on S. avenae. However, AChE activity decreased in both R. padi and S. avenae treated by the LC₂₅ of pirimicarb. We demonstrated sublethal and transgenerational effects of pirimicarb in the two wheat aphid species; it hinted at the importance of considering sublethal effects (including hormesis) of pirimicarb for optimizing Integrated Pest Management (IPM) of wheat aphids.     

Costs and benefits of hydroxamic acids-related resistance in winter wheat against the bird cherry-oat aphid, Rhopalosiphum padi L.

Estimations of infestation by the bird cherry-oat aphid (Rhopalosiphum padi) as well as measurements of grain yield in 26 Hungarian winter wheat cultivars under field conditions were correlated with the concentration of hydroxamic acids (Hx) in seedlings of those cultivars. The significant inverse relationship between infestation ratings and Hx levels in wheat showed that Hx, despite their decreased accumulation at later plant phenological stages, may be able to confer resistance against aphid infestation in the field. Since no significant relationship was found between grain yield and Hx levels in plants it is suggested that Hx accumulation does not impose a cost to the plant in terms of yield. These findings support earlier claims stressing the potential of Hx as breeding targets for aphid resistance in wheat.     

Searching for wheat resistance to aphids and wheat bulb fly in the historical Watkins and Gediflux wheat collections

Insect pests can reduce wheat yield by direct feeding and transmission of plant viruses. Here we report results from laboratory and field phenotyping studies on a wide range of wheat, including landraces from the Watkins collection deriving from before the green revolution, more modern cultivars from the Gediflux collection (north‐western Europe) and modern UK Elite varieties, for resistance to the bird cherry‐oat aphid, Rhopalosiphum padi (Homoptera: Aphididae) and the English grain aphid, Sitobion avenae (Homoptera: Aphididae). A total of 338 lines were screened for R. padi and 340 lines for S. avenae. Field trials were also conducted on 122 Watkins lines to identify wheat bulb fly, Delia coarctata, preference on these landraces. Considerable variation was shown in insect performance among and within different wheat collections, with reduced susceptibility in a number of varieties, but phenotyping did not identify strong resistance to aphids or wheat bulb fly. Field trials showed within collection differences in aphid performance, with fewer aphids populating lines from the Watkins collection. This differs from development data in laboratory bioassays and suggests that there is a pre‐alighting cue deterring aphid settlement and demonstrates differences in aphid preference and performance on older plants in the field compared with seedlings in the laboratory, highlighting the need for phenotyping for aphid resistance at different plant growth stages. No association was identified between performance of the different insect species on individual varieties, potentially suggesting different nutritional requirements or resistance mechanisms.     

Participation of the enzymes involved in the biosynthesis of biogenic amines in biochemical interactions between wheat (Triticum aestivum; Poaceae) and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae)

The studies concerned changes in the activities of ornithine decarboxylase (ODC), lysine decarboxylase (LDC) and tyrosine decarboxylase (TyDC) in tissues of wheat (Triticum aestivum L.) infested with bird cherry-oat aphid (Rhopalosiphum padi L.).Obtained results showed that the activities of the enzymes were stimulated in the less susceptible wheat Kontesa cv. infested by the aphids. In the case of the more susceptible Tonacja cv., on most occasions a decrease in the enzyme activities occurred. Such responses were especially clear for TyDC in both analysed cvs., and for LDC and ODC in the case of Kontesa cv. Thus it may be concluded that amino acid decarboxylation plays an important part in the biochemical defence developed in wheat tissues in response to R. padi infestation. The changes in the activities of the decarboxylases were dependent on the wheat genotype as well as the duration of the infestation.     

Participation of amino acid decarboxylases in biochemical interactions between triticale (Triticosecale; Poaceae) and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae)

The roles of ornithine decarboxylase, lysine decarboxylase and tyrosine decarboxylase in biochemical interactions of two cultivars of winter triticale (Triticosecale), Tornado and Witon, and bird cherry-oat aphid (Rhopalosiphum padi L.) were determined. Results showed the resistant Witon had higher lysine decarboxylase activity than the susceptible Tornado. There was a significant negative correlation between the density of R. padi populations and lysine decarboxylase activity. Such correlations did not occur for the other decarboxylases. Aphid feeding induced a decrease of lysine decarboxylase activity within both cultivars after one week of infestation and increased its activity after two weeks in the moderately resistant Witon. Ornithine decarboxylase activity was induced in tissues of the susceptible Tornado and inhibited in Witon after two weeks of infestation. Aphid infestations did not change tyrosine decarboxylase activity in Witon, whereas in Tornado it decreased in activity after one day of aphid feeding and then increased after two weeks. It was concluded that of the three enzymes studied, lysine decarboxylase was the most important in the response of winter triticale to infestation by R. padi.     

A novel theta-class glutathione S-transferase gene in Rhopalosiphum padi (L.) (Hemiptera: Aphididae): Identification,recombinant protein expression and function analyses of RpGSTT1

Glutathione S-transferases (GSTs) play a major role in the detoxification of insecticides and the protection against oxidative damage caused by ROS (reactive oxygen species). The bird cherry-oat aphid, Rhopalosiphum padi (L.), is a major crop pest worldwide. Chemical insecticides are currently used to control aphids, but insecticide resistance is an evolutionary issue for aphid control. In this research, we identified and cloned the full-length cDNA of a theta-class GST gene (RpGSTT1) from R. padi, which contains 702 bp open reading frame encoding 233 amino acids. RpGSTT1 was clustered together with theta classe of insect GSTs in the phylogenetic tree. Effect of insecticide exposure on the GST enzyme activity was investigated in vivo. After affinity purification, the recombinant RpGSTT1 protein was able to catalyze the conjugation of 1-chloro-2, 4-dinitrobenzene (CDNB). A disc diffusion assay showed that the RpGSTT1 can increase resistance to cumene hydroperoxide-induced oxidative stress. In addition, the purified recombinant RpGSTT1 protected super-coiled DNA from oxidative damage. By quantitative PCR, The relative expression level of RpGSTT1 in the aphid was highly up-regulated after 12 h exposure to β-cypermethrin, isoprocarb, malathion and sulfoxaflor, respectively. To our knowledge, RpGSTT1 is the first theta class of GST gene reported in bird cherry-oat aphid. Our findings indicate that RpGSTT1 may be involved in insecticide detoxification in R. padi.     

Hydroxamic acids affecting barley yellow dwarf virus transmission by the aphid Rhopalosiphum padi

2,4-Dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), a hydroxamic acid (Hx) occurring in wheat, was shown to deter feeding by the aphid Rhopalosiphum padi (L.), and to reduce BYDV transmission to the plant. Dual choice tests with wheat leaves showed the preferential settlement of aphids on leaves with lower levels of DIMBOA. Electric monitoring of aphid feeding behaviour showed that in seedlings with higher DIMBOA levels fewer aphids reached the phloem and they needed longer times to contact a phloem vessel than in those with lower levels. When aphids carrying BYDV were allowed to feed on wheat cultivars with different DIMBOA levels, fewer plants were infected with BYDV in the higher DIMBOA cultivars than in the lower ones. Preliminary field experiments showed a tendency for wheat cultivars with higher Hx levels to be more tolerant to infection by BYDV than lower Hx level ones.     

Resistance of apple cultivars to Dysaphis plantaginea (Hemiptera: Aphididae): role of tree phenology in infestation avoidance

To test the importance of flowering phenology in damage caused to apple cultivars by rosy apple aphid, Dysaphis plantaginea (Passerini) (Hemiptera: Aphididae), susceptibility of 16 cultivars was compared in greenhouse conditions after infestation with aptera and in the field after natural tree colonization. Flowering phenology was recorded in the field for all the cultivars. In both greenhouse and field trials, there were differences among cultivars with respect to aphid infestation and damage. However, damage in the greenhouse and field was not significantly correlated. Flowering phenology was also different among cultivars. Flowering order among cultivars was significantly negatively correlated with aphid infestation and damage in field, i.e., early leafing cultivars showed higher infestation and damage than late-leafing cultivars. If egg hatching occurs before bud bursting, neonate larvae will suffer a high mortality because they cannot feed on these late cultivars. A later recolonization of these trees is hampered because (1) winged aphids cannot live on apple but only on the secondary host, (2) apterous forms have a limited dispersal capability, and (3) aphid predators progressively increase in the orchard. Therefore, synchronization between egg hatching and bud bursting is of critical importance in the success or failure of infestation.     

Resistance and susceptibility of some wheat lines to bird cherry-oat aphid <Emphasis Type="Italic">Rhopalosiphum padi</Emphasis> (Hemiptera: Aphididae)

Bird cherry-oat aphid, Rhopalosiphum padi (L.), is one of the most serious pests of cereals, with an almost worldwide distribution. A primary screening test was carried out to gauge the resistance or susceptibility of 40 wheat lines to R. padi, and follow-up experiments were conducted to determine the development and fecundity rates of R. padi on eight lines. The forty wheat lines examined were classified into two major classes and four subclasses: A (e.g., ERWYT 87-1) and B (e.g., ERWYT 87-20, ERWYT 87-11), with the highest average number of aphids 14 days after infestation, subclass C (e.g., ERWYT 88-8, ERWYT 87-6, ERWYT 87-4), with the lowest average number of aphids, and subclass D (e.g., ERWYT 88-12, ERWYT 88-13), with intermediate status. Aphid nymph developmental time and survival both differed among the wheat lines. Differences were also observed in the fecundity of R. padi, the intrinsic rate of increase (r _m), and other parameters among the wheat lines tested. The highest and lowest values of r _m were obtained for ERWYT 87-1 and ERWYT 88-8 (0.36 and 0.26 nymphs/female/day, respectively). Three lines (ERWYT 87-4, ERWYT 87-6, ERWYT 88-8) were relatively resistant to R. padi, which could prove useful in the development of IPM programs for this aphid in wheat fields.     

Effects of Aphis fabae and Uromyces viciae-favae on the growth of a susceptible and an aphid resistant cultivar of Vicia faba

Damaging effects of either black bean aphid (Aphis fabae), broad bean rust (Uromyces viciae-fabae), or the combination of both were investigated on a susceptible (cv. Diana) and an aphid resistant (cv. Bolero) cultivar of Vicia faba. When compared with rust, aphids caused greater reductions of root dry weight, shoot dry weight, leaf area, and mean relative growth rate. The mean unit leaf rate was also reduced whereas the leaf area ratio was not affected. The damage caused per aphid was highest on the susceptible cultivar. Rust induced damage did not differ between the cultivars. Concomitant infestation with both pests only resulted in additive damage. The population development of aphids was delayed on partially resistant plants. High temperature and rust infection reduced the total number of aphids the plants were able to support but not the level of resistance. Thus the specific damaging effect per aphid was increased.     

Resistance to multiple cereal aphids in wheat–alien substitution and translocation lines

Rhopalosiphum padi, Schizaphis graminum, and Sitobion avenae are three of the most destructive aphid species of wheat (Triticum aestivum L.). They can significantly reduce wheat yields directly by feeding and indirectly by transmitting viruses. This study aimed to search for resistance to these aphid species among lines derived from different rye (Secale cereale) origins and from Aegilops speltoides, all in the genetic background of the wheat cultivar Pavon F76. Resistance was quantified as aphid weight (R. padi, S. avenae, and S. graminum) and the number of aphids and percentage of infested leaf area exhibiting chlorosis (S. graminum). The most resistant genotypes reduced R. padi and S. avenae weight by 24.2 and 34.3 %, respectively, at the seedling stage, compared with Pavon F76 control plants. Strong S. graminum resistance was found only in A. speltoides-derived lines, the most resistant of which (7A.7S-L5) sustained just 3 % chlorosis and reduced S. graminum colony weight by 67.7 %. One line carrying the 1AL.1RS_am wheat–rye translocation from Amigo wheat (originally from Insave rye) reduced S. avenae weight by 23.2 and 21.8 % in seedling and adult plants, respectively. Single genotypes carrying the complete 1R chromosome or the 1RS chromosome arm derived from E12165 wheat and Presto triticale proved to be resistant to both R. padi and S. avenae at the seedling stage. Further research should be conducted to unravel the genetic basis of resistance to these aphids in 1RS genotypes. The sources of resistance identified here may be useful for incorporating multiple aphid species resistance in wheat breeding programs, particularly for R. padi and S. avenae, to which no resistant wheats have been bred.     

Triticum monococcum lines with distinct metabolic phenotypes and phloem‐based partial resistance to the bird cherry–oat aphid Rhopalosiphum padi

Crop protection is an integral part of establishing food security, by protecting the yield potential of crops. Cereal aphids cause yield losses by direct damage and transmission of viruses. Some wild relatives of wheat show resistance to aphids but the mechanisms remain unresolved. In order to elucidate the location of the partial resistance to the bird cherry–oat aphid, Rhopalosiphum padi, in diploid wheat lines of Triticum monococcum, we conducted aphid performance studies using developmental bioassays and electrical penetration graphs, as well as metabolic profiling of partially resistant and susceptible lines. This demonstrated that the partial resistance is related to a delayed effect on the reproduction and development of R. padi. The observed partial resistance is phloem based and is shown by an increase in number of probes before the first phloem ingestion, a higher number and duration of salivation events without subsequent phloem feeding and a shorter time spent phloem feeding on plants with reduced susceptibility. Clear metabolic phenotypes separate partially resistant and susceptible lines, with the former having lower levels of the majority of primary metabolites, including total carbohydrates. A number of compounds were identified as being at different levels in the susceptible and partially resistant lines, with asparagine, octopamine and glycine betaine elevated in less susceptible lines without aphid infestation. In addition, two of those, asparagine and octopamine, as well as threonine, glutamine, succinate, trehalose, glycerol, guanosine and choline increased in response to infestation, accumulating in plant tissue localised close to aphid feeding after 24 h. There was no clear evidence of systemic plant response to aphid infestation.     

Olfactory responses of Rhopalosiphum padi to three maize,potato, and wheat cultivars and the selection of prospective crop border plants

Understanding host plant volatile – aphid interactions can facilitate the selection of crop border plants as a strategy to reduce plant virus incidence in crops. Crop border plant species with attractive odours could be used to attract aphids into the border crop and away from the main crop. As different cultivars of the same crop can vary in their olfactory attractiveness to aphids, selecting an attractive cultivar as a border crop is important to increase aphid landing rates. This study evaluated olfactory responses of the bird cherry‐oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), to three cultivars each of maize [Zea mays L. (Poaceae)], potato [Solanum tuberosum L. (Solanaceae)], and wheat [Triticum aestivum L. (Poaceae)] with the aim of selecting an attractive crop border plant to reduce the incidence of the non‐persistent Potato virus Y [PVY (Potyviridae)] in seed potatoes. Volatiles emitted by the crop cultivars were collected and identified using coupled gas chromatography/mass spectrometry. Quantitative and qualitative differences were found among cultivars. Behavioural responses of alate R. padi to odours of the cultivars and synthetic compounds identified from the plants were determined with a four‐arm olfactometer. Rhopalosiphum padi was attracted to odours emitted from maize cultivar 6Q‐121, but did not respond to odours from the remaining eight crop cultivars. Volatile compounds from maize and wheat cultivars that elicited a behavioural response from R. padi and contributed to differences in plant volatile profiles included (Z)‐3‐hexenyl acetate (attractant) and α‐farnesene, (E)‐2‐hexenal, indole, and (3E,7E)‐4,8,12‐trimethyltrideca‐1,3,7,11‐tetraene (TMTT) (repellents). We conclude that maize cv. 6Q‐121 is potentially suitable as a crop border plant based on the behavioural response of R. padi to the olfactory cues emitted by this cultivar. The findings provide insight into selecting crop cultivars capable of attracting R. padi to crop border plants.     

Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity

The symbiosis between grasses and endophytic fungi is a common phenomenon and can affect herbivore performance through acquired, chemical plant defence by fungal alkaloids. In laboratory experiments, two species of common grass aphids, Rhopalosiphum padi and Metopolophium dirhodum were tested, in a population experiment (on four plant cultivars) and individually (on one plant cultivar) for the effects of the endophyte, Neotyphodium lolii, that forms symbiotic associations with perennial ryegrass Lolium perenne. In the population experiment that lasted for four aphid generations both aphid species showed decreased population sizes when feeding on each of the four endophyte-infected cultivars. Individuals of R. padi tested individually showed reduced adult life span and fecundity when feeding on infected plants. Individuals of M. dirhodum showed no response in any of the traits measured. This suggests that R. padi individuals are more sensitive to endophyte infection than M. dirhodum individuals. However, all infected grass cultivars reduced population sizes of both aphid species over four generations. Therefore, fungal endophytes can reduce populations of aphid herbivores independent of plant cultivars.     

Evaluation of lycosid,micryphantid and linyphiid spiders as predators ofRhopalosiphum padi (Hom.: Aphididae) and their functional response to prey density-laboratory experiments

Laboratory experiments were performed to determine the potential of dominant spider species in winter wheat in Germany,Erigone atra (Blackwall),Lepthyphantes tenuis (Blackwall) andPardosa agrestis (Westring) adults and youngs, in suppressing the population ofRhopalosiphum padi (L.) on wheat plants and their functional response to different aphid densities. The presence of spiders significantly caused between 34 and 58% reduction in aphid population development on wheat plants compared to the aphid population in the absence of spiders. The functional response curves for these spiders as predators ofR. padi seem to descrive a typical type II functional response with the prey consumed increasing to a plateau as aphid densities increased. Prey killed without eating was linear on prey density.     

Sources of variation in the interaction between three cereal aphids (Hemiptera: Aphididae) and wheat (Poaceae)

The relative contributions of host plant, herbivore species and clone to variation in the interaction between cereal aphids and wheat were investigated using five clones each of three species, Rhopalosiphum padi (Linnaeus), Sitobion avenae (Fabricius) and Schizaphis graminum (Rondani), on seedlings of two cultivars of Triticum aestivum L. and one cultivar of Triticum durum Desf. More individuals and biomass of R. padi than of the other two species were produced on seedlings. The three wheat cultivars lost similar amounts of biomass as a result of infestation by aphids, with the amount lost depending on aphid species: S. avenae caused the lowest loss in biomass. Variation in aphid biomass production was due mostly to differences among aphid species (70%), less to the interaction between wheat type and aphid species (7%), and least to aphid clone (1%). The specific impact of the aphids on the plants ranged from 1.7 to 3.7 mg of plant biomass lost per mg of aphid biomass gained, being lowest for R. padi and highest for S. graminum. Variation in plant biomass lost to herbivory was due mostly to unknown sources of error (95%), probably phenotypic differences among individual seedlings, with 3% due to aphid species and none attributable to aphid clone. For these aphid-plant interactions, differences among aphid clones within species contributed little to variation in aphid and plant productivity; therefore, a small sample of clones was adequate for quantifying the interactions. Furthermore, one clone of each species maintained in the laboratory for about 200 parthenogenetic generations was indistinguishable from clones collected recently from the field.     

Morphological observations on the preimaginal stages ofAphelinus varipes (Hym., Aphelinidae) and the effects of this parasitoid on the aphidRhopalosiphum padi (Hom., Aphididae)

Three instar larvae could be observed forAphelinus varipes. In the second and third instars, the colon which forms the largest part of the hindgut was composed of secretory cells. There was a reduction in the size and number of embryos produced by parasitized aphids. Fat cells of parasitized aphids also degenerated sooner than those of unparasitized aphids. The number of mycetocytes remained higher in parasitizedRhopalosiphum padi than in non-parasitized aphids. During the last instar ofA. varipes the host aphid developed into a mummy in which black pigments were incorporated into the exocuticle and the integument of the aphid became sclerotized.     

Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies

This study investigated the effects of airborne interaction between different barley cultivars on the behaviour of bird cherry-oat aphid Rhopalosiphum padi, the ladybird Coccinella septempunctata and the parasitoid Aphidius colemani. In certain cultivar combinations, exposure of one cultivar to air passed over a different cultivar caused barley to have reduced aphid acceptance and increased attraction of ladybirds and parasitoids. Parasitoids attacked aphids that had developed on plants under exposure more often than those from unexposed plants, leading to a higher parasitisation rate. Ladybirds, but not parasitoids, were more attracted to combined odours from certain barley cultivars than either cultivar alone. The results show that airborne interactions between undamaged plants can affect higher trophic levels, and that odour differences between different genotypes of the same plant species may be sufficient to affect natural enemy behaviour.